Artículo

Ferreira, J.L.R.; Lonné, M.N.; França, T.A.; Maximilla, N.R.; Lugokenski, T.H.; Costa, P.G.; Fillmann, G.; Antunes Soares, F.A.; de la Torre, F.R.; Monserrat, J.M. "Co-exposure of the organic nanomaterial fullerene C60 with benzo[a]pyrene in Danio rerio (zebrafish) hepatocytes: Evidence of toxicological interactions" (2014) Aquatic Toxicology. 147:76-83
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Compounds from the nanotechnology industry, such as carbon-based nanomaterials, are strong candidates to contaminate aquatic environments because their production and disposal have exponentially grown in a few years. Previous evidence shows that fullerene C60, a carbon nanomaterial, can facilitate the intake of metals or PAHs both in vivo and in vitro, potentially amplifying the deleterious effects of these toxicants in organisms. The present work aimed to investigate the effects of fullerene C60 in a Danio rerio (zebrafish) hepatocyte cell lineage exposed to benzo[a]pyrene (BaP) in terms of cell viability, oxidative stress parameters and BaP intracellular accumulation. Additionally, a computational docking was performed to investigate the interaction of the fullerene C60 molecule with the detoxificatory and antioxidant enzyme πGST. Fullerene C60 provoked a significant (p<0.05) loss in cellular viability when co-exposed with BaP at 0.01, 0.1 and 1.0μg/L, and induced an increase (p<0.05) in BaP accumulation in the cells after 3 and 4h of exposure. The levels of reactive oxygen species (ROS) in the cells exposed to BaP were diminished (p<0.05) by the fullerene addition, and the increase of the GST activity observed in the BaP-only treated cells was reduced to the basal levels by co-exposure to fullerene. However, despite the potential of the fullerene molecule to inhibit π GST activity, demonstrated by the computational docking, the nanomaterial did not significantly (p>0.05) alter the enzyme activity when added to GST purified extracts from the zebrafish hepatocyte cells. These results show that fullerene C60 can increase the intake of BaP into the cells, decreasing cell viability and impairing the detoxificatory response by phase II enzymes, such as GST, and this latter effect should be occurring at the transcriptional level. © 2013 Elsevier B.V.

Registro:

Documento: Artículo
Título:Co-exposure of the organic nanomaterial fullerene C60 with benzo[a]pyrene in Danio rerio (zebrafish) hepatocytes: Evidence of toxicological interactions
Autor:Ferreira, J.L.R.; Lonné, M.N.; França, T.A.; Maximilla, N.R.; Lugokenski, T.H.; Costa, P.G.; Fillmann, G.; Antunes Soares, F.A.; de la Torre, F.R.; Monserrat, J.M.
Filiación:Universidade Federal do Rio Grande-FURG, Instituto de Ciências Biológicas (ICB), Campus Carreiros, Av. Itália km 8 s/n (96200-970), Rio Grande, RS, Brazil
Fisiologia Animal Comparada, Instituto de Ciências Biológicas (ICB), FURG, Brazil
Laboratório de Microcontaminantes Orgânicos e Ecotoxicologia Aqua., Instituto de Oceanografia (IO), FURG, Brazil
Rede de Nanotoxicologia (MCTI/CNPq), Nanotoxi. ocup. e ambiental: subsidios cientificos para estabelecer marcos reg. e aval. de riscos, Rio Grande, RS, Brazil
Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Buenos Aires, Argentina
Universidade Federal de Santa Maria (UFSM), Departamento de Química, Santa Maria, RS, Brazil
Universidad Nacional de Luján, Departamento de Ciencias Básicas, Buenos Aires, Argentina
Instituto Nacional de Ciência e Tecnologia de Nanomateriais de Carbono (CNPq), Brazil
Palabras clave:BaP; Delivery; GST; Nanotoxicology; Synergistic effect; benzo[a]pyrene; fullerene; glutathione transferase; nanomaterial; reactive oxygen metabolite; antioxidant; bioaccumulation; cyprinid; enzyme activity; fullerene; nanotechnology; pollution effect; pollution exposure; pyrene; toxicology; viability; animal cell; article; bioaccumulation; cell viability; chemical interaction; concentration response; controlled study; detoxification; enzyme activity; liver cell; molecular docking; nonhuman; oxidative stress; priority journal; water contamination; zebra fish; BaP; Delivery; GST; Nanotoxicology; Synergistic effect; Animals; Benzo(a)pyrene; Cell Survival; Fullerenes; Hepatocytes; Oxidative Stress; Reactive Oxygen Species; Water Pollutants, Chemical; Zebrafish
Año:2014
Volumen:147
Página de inicio:76
Página de fin:83
DOI: http://dx.doi.org/10.1016/j.aquatox.2013.12.007
Título revista:Aquatic Toxicology
Título revista abreviado:Aquat. Toxicol.
ISSN:0166445X
CODEN:AQTOD
CAS:benzo[a]pyrene, 50-32-8; glutathione transferase, 50812-37-8
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_0166445X_v147_n_p76_Ferreira

Referencias:

  • Acosta, D.S., Kneip, F.C., Alves de Almeida, E., Ventura-Lima, J., Monserrat, J.M., Geracitano, L.A., Fullerene and omega-3 and omega-6 fatty acids on fish brain antioxidant status (2012) Fish Physiology and Biochemistry, 38, pp. 1477-1485
  • Adini, A.R., Redlich, M., Tenne, R., Medical applications of inorganic fullerene-like nanoparticles (2011) Journal of Materials Chemistry, 21, p. 15121
  • Alsop, D., Brown, S., Van Der Kraak, G., The effects of copper and benzo[a]pyrene on retinoids and reproduction in zebrafish (2007) Aquatic Toxicology, 82, pp. 281-295
  • Al-Subiai, N., Arlt, V.M., Frickers, P.E., Readman, J.W., Stolpe, B., Lead, J.R., Moody, A.J., Jha, A.N., Merging nano-genotoxicology with eco-genotoxicology: an integrated approach to determine interactive genotoxic and sub-lethal toxic effects of C60 fullerenes and fluoranthene in marine mussels, Mytilus sp. (2012) Mutation Research, 745, pp. 92-103
  • Andrievsky, G.V., Klochkov, V.K., Bordyuh, A.B., Dovbeshko, G.I., Comparative analysis of two aqueous-colloidal solutions of C60 fullerene with help of FTIR reflectance and UV-vis spectroscopy (2002) Chemical Physics Letters, 364, pp. 8-17
  • Andrievsky, G.V., Bruskov, V.I., Tykhomyrov, A.A., Gudkov, S.V., Peculiarities of the antioxidant and radioprotective effects of hydrated C60 fullerene nanostuctures in vitro and in vivo (2009) Free Radical Biology & Medicine, 47, pp. 786-793
  • Aschberger, K., Micheletti, C., Sokull-Klüttgen, B., Christensen, F.M., Analysis of currently available data for characterising the risk of engineered nanomaterials to the environment and human health-lessons learned from four case studies (2011) Environment International, 37, pp. 1143-1156
  • Baun, A., Sørensen, S.N., Rasmussen, R.F., Hartmann, N.B., Koch, C.B., Toxicity and bioaccumulation of xenobiotic organic compounds in the presence of aqueous suspensions of aggregates of nano-C60 (2008) Aquatic Toxicology, 86, pp. 379-387
  • Britto, R.S., Garcia, M.L., da Rocha, A.M., Flores, J.A., Pinheiro, M.V.B., Monserrat, J.M., Ferreira, J.L.R., Effects of carbon nanomaterials fullerene C60 and fullerol C60 (OH)18-22 on gills of fish Cyprinus carpio (Cyprinidae) exposed to ultraviolet radiation (2012) Aquatic Toxicology, 114-115, pp. 80-87
  • Castorena-Torres, F., De León, M., Cisneros, B., Zapata-Perez, O., Salinas, J., Albores, A., Changes in gene expression induced by polycyclic aromatic hydrocarbons in the human cell lines HepG2 and A549 (2008) Toxicology in Vitro, 22, pp. 411-421
  • Chang, L.W., Chang, Y., Ching, H., Chi, C., Tsai, M., Hsien, L.P., Increase of carcinogenic risk via enhancement of cyclooxygenase-2 expression and hydroxyestradiol accumulation in human lung cells as a result of interaction between BaP and 17-beta estradiol (2007) Carcinogenesis, 28, pp. 1606-1612
  • Cho, Y.-J., Ahn, T.K., Song, H., Kim, K.S., Lee, C.Y., Seo, W.S., Lee, K., Park, J.T., Unusually high performance photovoltaic cell based on a [60]fullerene metal cluster porphyrin dyad SAM on an ITO electrode (2005) Journal of the American Chemical Society, 127, pp. 2380-2381
  • Christian, P., Von der Kammer, F., Baalousha, M., Hofmann, T., Nanoparticles: structure, properties, preparation and behaviour in environmental media (2008) Ecotoxicology, 17, pp. 326-343
  • Costa, C.L.A., Chaves, I.S., Ventura-Lima, J., Ferreira, J.L.R., Ferraz, L., Carvalho, L.M.D., Monserrat, J.M., In vitro evaluation of co-exposure of arsenium and an organic nanomaterial (fullerene, C60) in zebrafish hepatocytes (2012) Comparative Biochemistry and Physiology C, 155, pp. 206-212
  • Ehrenberg, M.S., Friedman, A.E., Finkelstein, J.N., Oberdörster, G., McGrath, J.L., The influence of protein adsorption on nanoparticle association with cultured endothelial cells (2009) Biomaterials, 30, pp. 603-610
  • Fako, V.E., Furgeson, D.Y., Zebrafish as a correlative and predictive model for assessing biomaterial nanotoxicity (2009) Advanced Drug Delivery Reviews, 61, pp. 478-486
  • Fan, W., Cui, M., Liu, H., Wang, C., Shi, Z., Tan, C., Yang, X., Nano-TiO2 enhances the toxicity of copper in natural water to Daphnia magna (2011) Environmental Pollution, 159, pp. 729-734
  • Ferreira, J.R.F., Barros, D.M., Geracitano, L.A., Fillmann, G., Fossa, C.E., De Almeida, E.A., Prado, M.C., Monserrat, J.M., Influence of in vitro exposure to fullerene C60 in redox state and lipid peroxidation of brain and gills of carp Cyprinus carpio (Cyprinidae) (2012) Environmental Toxicology and Chemistry, 31, pp. 961-967
  • Filgueira, D.M.V.B., de Freitas, P.S., Souza Votto, A.P., Fillmann, G., Monserrat, J.M., Geracitano, L.A., Trindade, G.S., Photodynamic action of benzo[a]pyrene in K562 cells (2007) Photochemistry and Photobiology, 83, pp. 1-6
  • Fraser, T.K., Reinardy, H., Shaw, C., Henry, B.J., Handy, T.B.R.D., Dietary toxicity of single-walled carbon nanotubes and fullerenes (C60) in rainbow trout (Oncorhynchus mykiss) (2011) Nanotoxicology, 5 (1), pp. 98-108
  • Ganji, M.D., Yazdani, H., Mirnejad, A., B36N36 fullerene-like nanocages: a novel material for drug delivery (2010) Physica E: Low-dimensional Systems and Nanostructures, 42, pp. 2184-2189
  • Garner, L.V.T., Di Giulio, R.T., Glutathione transferase pi class 2 (GSTp2) protects against the cardiac deformities caused by exposure to PAHs but not PCB-126 in zebrafish embryos (2012) Comparative Biochemistry and Physiology C, 155, pp. 573-579
  • Goyal, R.N., Gupta, V.K., Sangal, A., Bachheti, N., Voltammetric determination of uric acid at a fullerene-C60-modified glassy carbon electrode (2005) Electroanalysis, 17, pp. 2217-2223
  • Habig, W.H., Jakoby, W.B., Assays for differentiation of glutathione S-transferases (1981) Methods in Enzymology, 77, pp. 398-405
  • Henry, T.B., Menn, F.M., Fleming, J.T., Wilgus, J., Compton, R.N., Sayler, G.S., Attributing effects of aqueous C60 nano-aggregates to tetrahydrofuran decomposition products in larval zebrafish by assessment of gene expression (2007) Environmental Health Perspectives, 115, pp. 1059-1065
  • Henry, T.B., Petersen, E.J., Compton, R.N., Aqueous fullerene aggregates (nC60) generate minimal reactive oxygen species and are of low toxicity in fish: a revision of previous reports (2011) Current Opinion in Biotechnology, 22, pp. 533-537
  • Ji, X., Tordova, M., O'Donnell, R., Parsons, J.F., Hayden, J.B., Gilliland, G.L., Zimniak, P., Structure and function of the xenobiotic substrate-binding site and location of a potential non-substrate-binding site in a class π glutathione S-transferase (1997) Biochemistry, 36, pp. 9690-9702
  • Kahru, A., Dubourguier, H.-C., From ecotoxicology to nanoecotoxicology (2010) Toxicology, 269, pp. 105-119
  • Khokhryakov, A., Avdeev, M., Aksenov, V., Bulavin, L., Structural organization of colloidal solution of fullerene C60 in water by data of small angle neutron scattering (2006) Journal of Molecular Liquids, 127, pp. 73-78
  • Kurelec, B., Krca, S., Garg, A., Gupta, R.C., The potential of carp to bioactivate benzo[a]pyrene metabolites that bind to DNA (1991) Cancer Letters, 57, pp. 255-260
  • Limbach, L.K., Wick, P., Exposure of engineered nanoparticles to human lung epithelial cells: influence of chemical composition and catalytic activity on oxidative stress (2007) Environmental Science & Technology, 41, pp. 4158-4163
  • Lyon, D.Y., Adams, L.K., Falkner, J.C., Alvarez, P.J.J., Antibacterial activity of fullerene water suspensions: effects of preparation method and particle size (2006) Environmental Science & Technology, 40, pp. 4360-4366
  • Mao, J., Wang, L., Qian, Z., Tu, M., Uptake and cytotoxicity of Ce(IV) doped TiO2 nanoparticles in human hepatocyte cell line L02 (2010) Journal of Nanomaterials, 2010, pp. 1-8
  • Mashino, T., Okuda, K., Hirota, T., Hirobe, M., Nagano, T., Mochizuki, M., Inhibitory effects of fullerene derivatives on glutathione reductase (2001) Fullerene Science and Technology, 9, pp. 191-196
  • Murdock, R.C., Braydich-Stolle, L., Schrand, A.M., Schlager, J.J., Hussain, S.M., Characterization of nanomaterial dispersion in solution prior to in vitro exposure using dynamic light scattering technique (2008) Toxicological Sciences, 101, pp. 239-253
  • Nakashima, N., Tokunaga, T., Nonaka, Y., Nakanishi, T., Murakami, H., Sagara, T., A fullerene/lipid electrode device: reversible electron transfer reaction of C60 embedded in a cast film of an artificial ammonium lipid on an electrode in aqueous solution (1998) Angewandte Chemie International Edition, 37, pp. 2671-2673
  • Naspinski, C., Gu, X., Zhou, G.-D., Mertens-Talcott, S.U., Donnelly, K.C., Tian, Y., Pregnane X receptor protects HepG2 cells from BaP-induced DNA damage (2008) Toxicological Sciences, 104, pp. 67-73
  • Oberdörster, E., Manufactured nanomaterials (fullerenes C60) induce oxidative stress in the brain of juvenile largemouth bass (2004) Environmental Health Perspectives, 112, pp. 1058-1062
  • Palanikumar, L., Kumaraguru, A.K., Ramakritinan, C.M., Anand, M., Biochemical response of anthracene and benzo[a]pyrene in milkfish Chanos chanos (2012) Ecotoxicology and Environmental Safety, 75, pp. 187-197
  • Partha, R., Mitchell, L.R., Lyon, J.L., Joshi, P.P., Conyers, J.L., Buckysomes: fullerene-based nanocarriers for hydrophobic molecule delivery (2008) ACS Nano, 2, pp. 1950-1958
  • Pinteala, M., Dascalu, A., Ungurenasu, C., Binding fullerenol C60(OH)24 to dsDNA (2009) International Journal of Medicine, 4, pp. 193-199
  • Rose, R.L., Levi, P.E., Reactive metabolites (2004) A Textbook of Modern Toxicology, p. 158. , John Wiley & Sons, Inc., Hoboken, New Jersey, E. Hodgson (Ed.)
  • Sasco, A.J., Secretan, M.B., Straif, K., Tobacco smoking and cancer: a brief review of recent epidemiological evidence (2004) Lung Cancer, 45 (SUPPL. 2), pp. S3-S9
  • Santos, L.J., Gonçalves, A.S.P., Krambrock, K., Pinheiro, M.V.B., Eberlin, M.N., Vaz, B.G., de Freitas, R.P., Alves, R.B., Synthesis of fullerene derivatives bearing five-membered heterocyclic wings and an investigation of their photophysical kinetic properties (2011) Journal of Photochemistry and Photobiology A: Chemistry, 217, pp. 184-190
  • Sun, H., Zhang, X., Zhang, Z., Chen, Y., Crittenden, J.C., Influence of titanium dioxide nanoparticles on speciation and bioavailability or arsenite (2009) Environmental Pollution, 157, pp. 1165-1170
  • Tarabukina, E., Zoolshoev, Z., Melenevskaya, E., Budtova, T., Delivery of fullerene-containing complexes via microgel swelling and shear-induced release (2010) International Journal of Pharmaceutics, 384, pp. 9-14
  • Trpkovic, A., Todorovic-Markovic, B., Trajkovic, V., Toxicity of pristine versus functionalized fullerenes: mechanisms of cell damage and the role of oxidative stress (2012) Archives of Toxicology, 86, pp. 1809-1827
  • Walker, C.H.S., Hopkin, P., Sibly, R.M., Peakall, D.B., (2001) Principles of Ecotoxicology, , Taylor & Francis Inc., New York
  • Wang, D., Hu, J., Irons, D.R., Wang, J., Synergistic toxic effect of nano-TiO2 and As(V) on Ceriodaphnia dubia (2011) Science of the Total Environment, 409, pp. 1351-1356
  • Winzer, K., Winston, G.W., Becker, W., Van Noorden, C.J., Köehler, A., Sex-related responses to oxidative stress in primary cultured hepatocytes of European flounder (Platichthys flesus L) (2001) Aquatic Toxicology, 52, pp. 143-155
  • Vieira, L.R., Sousa, A., Frasco, M.F., Lima, I., Morgado, F., Guilhermino, L., Acute effects of benzo[a]pyrene, anthracene and a fuel oil on biomarkers of the common goby Pomatoschistus microps (Teleostei, Gobiidae) (2008) The Science of the Total Environment, 395, pp. 87-100
  • Xia, X.R., Monteiro-Riviere, N.A., Riviere, J.E., Intrinsic biological property of colloidal fullerene nanoparticles (nC60): lack of lethality after high dose exposure to human epidermal and bacterial cells (2010) Toxicology Letters, 197, pp. 128-134
  • Yang, X.Y., Edelmann, R.E., Oris, J.T., Suspended C60 nanoparticles protect against short-term UV and fluoranthene photo-induced toxicity, but cause long-term damage in Daphnia magna (2010) Aquatic Toxicology, 100, pp. 202-210
  • Zar, J.H., (1984) Biostatistical Analysis, , Prentice Hall, New Jersey

Citas:

---------- APA ----------
Ferreira, J.L.R., Lonné, M.N., França, T.A., Maximilla, N.R., Lugokenski, T.H., Costa, P.G., Fillmann, G.,..., Monserrat, J.M. (2014) . Co-exposure of the organic nanomaterial fullerene C60 with benzo[a]pyrene in Danio rerio (zebrafish) hepatocytes: Evidence of toxicological interactions. Aquatic Toxicology, 147, 76-83.
http://dx.doi.org/10.1016/j.aquatox.2013.12.007
---------- CHICAGO ----------
Ferreira, J.L.R., Lonné, M.N., França, T.A., Maximilla, N.R., Lugokenski, T.H., Costa, P.G., et al. "Co-exposure of the organic nanomaterial fullerene C60 with benzo[a]pyrene in Danio rerio (zebrafish) hepatocytes: Evidence of toxicological interactions" . Aquatic Toxicology 147 (2014) : 76-83.
http://dx.doi.org/10.1016/j.aquatox.2013.12.007
---------- MLA ----------
Ferreira, J.L.R., Lonné, M.N., França, T.A., Maximilla, N.R., Lugokenski, T.H., Costa, P.G., et al. "Co-exposure of the organic nanomaterial fullerene C60 with benzo[a]pyrene in Danio rerio (zebrafish) hepatocytes: Evidence of toxicological interactions" . Aquatic Toxicology, vol. 147, 2014, pp. 76-83.
http://dx.doi.org/10.1016/j.aquatox.2013.12.007
---------- VANCOUVER ----------
Ferreira, J.L.R., Lonné, M.N., França, T.A., Maximilla, N.R., Lugokenski, T.H., Costa, P.G., et al. Co-exposure of the organic nanomaterial fullerene C60 with benzo[a]pyrene in Danio rerio (zebrafish) hepatocytes: Evidence of toxicological interactions. Aquat. Toxicol. 2014;147:76-83.
http://dx.doi.org/10.1016/j.aquatox.2013.12.007